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Social Snakes? the Role of Kin Selection in Rattlesnake Aggregations Melissa Amarello1 and Jeffrey J

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Social Snakes? the Role of Kin Selection in Rattlesnake Aggregations Melissa Amarello1 and Jeffrey J LOCAL RESEARCH NEWS Social Snakes? The role of kin selection in rattlesnake aggregations Melissa Amarello1 and Jeffrey J. Smith2 1School of Life Sciences, Arizona State University, Tempe, Arizona, USA; [email protected] 2The Nature Conservancy, 6502 N Muleshoe Ranch RD, Willcox, Arizona, USA; [email protected] Studies of animal sociality have long challenged our understanding of evolution and provoked some of the greatest debates in the field. Although sociality takes a variety of forms, researchers have historically selected the most extreme forms of eusocial- ity and cooperative taxa for intensive study (Ebensperger 2001, Cahan et Studies of al. 2002, Davis et al. 2011, Clark et al. 2012). However, simpler, often over- animal sociality looked forms of sociality may better have long chal- inform us about the evolutionary causes and consequences of social lenged our un- behavior (Cahan et al. 2002, Chapple Figure 1. Yellow Man (center, adult male Crotalus cerberus) with several juveniles and derstanding of 2003, Davis et al. 2011). females basking at a den entrance. Photo by Melissa Amarello, April 2011. Aggregations (groups) of animals represent some plays a role in rattlesnake aggregations, pairs with high- evolution and of the simplest forms of sociality and may lead to the er association indices will be more related than pairs provoked some evolution of complex sociality (Graves and Duvall that do not spend much (or any) time together. 1995). Animals may aggregate for active (e.g., allo- Since April 2011, we have used remote timelapse of the greatest parenting, group defense, kin selection; Vonhof et cameras (Timelapse PlantCam and TimelapseCam debates in the al. 2004) or passive benefits (e.g., thermoregulation; 8.0, Wingscapes, Inc., Alabaster, AL, USA) to re- Graves and Duvall 1995). According to Hamilton’s cord behavior of C. cerberus in aggregations at a site field. Although rule, an individual can increase its fitness by helping near Prescott, Arizona. Some pregnant females, their sociality takes relatives (Hamilton 1964); thus, active and passive ben- offspring, and the occasional male aggregate at these efits of grouping may be enhanced by associating with sites during the summer active season (Amarello et al. a variety of kin (Vonhof et al. 2004, Davis et al. 2011). Kin-based 2011), but most aggregation behavior happens dur- forms, re- groups are widespread, but have only recently been ing the spring, so we focused our efforts during this described in lizards and snakes (Chapple 2003, Davis period (ca. mid-April through mid-May). We identified searchers have et al. 2011, Clark et al. 2012). 78 individual rattlesnakes (42 adults and 36 juveniles), historically se- Although typically regarded as asocial, some collected DNA samples from over 50, and observed rattlesnakes form aggregations (Graves and Duvall them a total of 531 times. lected the most 1995, Clark et al. 2012), recognize and preferentially To date, we have documented nonrandom pat- extreme forms associate with kin (Clark 2004, Clark et al. 2012), and terns of association in C. cerberus, suggesting that they possess traits linked to complex sociality: long lifespan, aggregate for active rather than passive benefits. Some of eusociality late maturation, and viviparity (Ebensperger 2001, rattlesnakes are more gregarious than others, and they and cooperative Chapple 2003). Rattlesnake aggregations are assumed are choosy about whom they associate with (Amarello to be resource-based because they usually occur in 2012). Our collaborator at the University of Arizona, taxa for inten- cool climates where habitat providing opportunities Dr. Hans-Werner Herrmann, identified 38 informa- sive study. to thermoregulate may be limited (Graves and Duvall tive microsatellite DNA markers for genotyping C. 1995). However, in the relatively warm climate of cerberus, so we can examine how relatedness affects the Arizona, Arizona Black Rattlesnakes (Crotalus cerberus) strength of these associations. aggregate at winter hibernacula and nesting sites. We are only beginning to understand the complex We hypothesize that C. cerberus preferentially aggre- social lives of rattlesnakes (Clark et al. 2012, Amarello gate with kin to increase their indirect fitness through 2012) and comparing the ecology of C. cerberus to aso- kin selection (Hamilton 1964). We will test the kin cial and social squamates will provide further informa- selection hypothesis by calculating relatedness and an tion on the evolution of sociality (Chapple 2003). But association index (percent time seen together) for each perhaps most important, our data are used to facilitate pair of rattlesnakes. We predict that, if kin selection snake conservation through education. Pernicious SONORAN HERPETOLOGIST 25 (12) 2012 129 myths and popular media that have long portrayed snakes as malicious villains instill and nurture fear of snakes, which has led to widespread persecution and obstruction to conservation efforts (Seigel and Mullin 2009). In contrast to how snakes are usually seen in the media, recent research on rattlesnakes reveals be- havior that appeals to the general public: parental care (Greene et al. 2002, Amarello et al. 2011), cooperation (Amarello et al. 2011), and social interactions (Clark et al. 2012, Amarello 2012). By revealing the social nature of rattlesnakes through live and virtual outlets (Amarello and Smith 2012), we are helping to change the public’s perception of snakes from “cold-blooded killer” to social creatures with complex family lives. Thanks to those who inspired, supported, and assisted us: M. Cardwell, R. Clark, D. DeNardo, M. Feldner, H. Greene, K. McGraw, J. Porter, R. Repp, By revealing B. Rogers, G. Schuett, M. Seward, J. Slone, B. Sullivan, Arizona Game and Fish Department (SP796730 and the social na- SP729143), and ASU IACUC. The Tucson Herpeto- ture of rattle- logical Society, National Science Foundation, Chicago Herpetological Society, Herpetologists’ League, Wing- snakes through scapes, and Rocket Hub supporters provided funding live and vir- for this project. tual outlets Literature Cited (Amarello and Amarello, M., J.J. Smith, and J. Slone. 2011. Family val- Smith 2012), ues: Maternal care in rattlesnakes is more than mere we are help- attendance. Available from Nature Precedings <dx. Figure 2. Barb (left, juvenile Crotalus cerberus) basking with doi.org/10.1038/npre.2011.6671.1> Flash (right, adult male) near a den. Photo by Melissa Amarello, ing to change Amarello, M., and J.J. Smith. 2012. SocialSnakes [blog]. April 2012. the public’s <blog.socialsnakes.org> London Series B 278:1507-1514. Amarello, M. 2012. Social Snakes? Non-random Ebensperger, L.A. 2001. A review of the evolutionary perception of association patterns detected in a population of causes of rodent group-living. Acta Theriologica snakes from Arizona black rattlesnakes (Crotalus cerberus). M.S. 46:115-144. Thesis, Arizona State University, Tempe. Graves, B.M., and D. Duvall. 1995. Aggregation of “cold-blooded Cahan, S.H., D.T. Blumstein, L. Sundström, J. Liebig, squamate reptiles associated with gestation, oviposi- killer” to social and A. Griffin. 2002. Social trajectories and the tion, and parturition. Herpetological Monographs evolution of social behavior. Oikos 96:206-216. 9:102-119. creatures with Chapple, D.G. 2003. Ecology, life-history, and behav- Greene, H.W., P. May, D.L. Hardy, Sr., J. M. Sciturro, complex family ior in the Australian Scincid genus Egernia, with and T. Farrell. 2002. Parental behavior by vipers. comments on the evolution of complex sociality in Pages 179-205 in: G.W. Schuett, M. Höggren, M.E. lives. lizards. Herpetological Monographs 17:145-180. Douglas, and H.W. Greene, editors. Biology of the Clark, R.W. 2004. Kin recognition in rattlesnakes. vipers. Eagle Mountain Publishing, Eagle Moun- Proceedings of the Royal Society of London Series tain, Utah, USA. B: Biological Sciences 271:S243-S245. Hamilton, W.D. 1964. The genetical evolution of social Clark, R.W., W.S. Brown, R. Stechert, and H.W. behaviour. I. Journal of Theoretical Biology 7:1-16. Greene. 2012. Cryptic sociality in rattlesnakes (Cro- Seigel, R.A., and S.J. Mullin. 2009. Snake conservation, talus horridus) detected by kinship analysis. Biology present and future. Pages 281-290 in: S.J. Mullin and Letters 8:523-525. R.A. Seigel, editors. Snakes: ecology and conserva- Croft, D.P., R. James, and J.Krause. 2008. Explor- tion. Cornell University Press, Ithaca, NY, USA. ing Animal Social Networks. Princeton University Vonhof, M.J., H. Whitehead, and M.B. Fenton. 2004. Press, Princeton, N.J., USA. Analysis of Spix’s disc-winged bat association Davis, A.R., A. Corl, Y. Surget-Groba, and B. Sinervo. patterns and roosting home ranges reveal a novel 2011. Convergent evolution of kin-based social- social structure among bats. Animal Behaviour ity in a lizard. Proceedings of the Royal Society of 68:507-521. SONORAN HERPETOLOGIST 25 (12) 2012 130.
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